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Hamilton, J. A.

Publications and source records attributed to Hamilton, J. A..

11 recordsLinked to original sources

Climate gradients drive the evolution of seed morphology and life history with impacts to seedling fitness in Fraxinus nigra

Background and AimsClimate gradients influence seed morphology, emergence, and early life-history traits with cumulative impacts to individual fitness. For ex situ seed collections, which represent an invaluable repository of potential trait information for species management and conservation, climate data can guide preservation of adaptive variation and inform deployment strategies for restoration. Here we leverage a range-wide ex situ seed collection of critically endangered black ash seeds (Fraxinus nigra) to evaluate how climatic gradients shape variation in morphology and early life-history. MethodsTo test how climate of origin, seed morphology, and early life-history interact to impact first year fitness, high-throughput X-ray imaging and neural network-based segmentation were used to quantify variation in seed morphology for 701 maternal lineages spanning 76 populations across the range of F. nigra. Following this, a subset of seeds were used to establish a common garden experiment and quantify variation in emergence, early life-history transitions, and their cumulative impact to first-year survival and growth. ResultsOn average, differences within-population explained [~]43% of the variability in seed morphology, while among-population differences explained [~]14%. This suggests that substantial genetic variation exists within populations for natural selection to act upon and differences have evolved among populations. Climate associations indicated warmer and drier environments predicted heavier seeds with faster developmental transitions and increased first-year height. Together, climate of origin, seed mass, and timing of developmental transitions best predicted cumulative fitness, with populations from more continental environments exhibiting greater survival and first-year height accumulation on average. ConclusionsOverall, these results highlight the importance of climate of origin, seed traits, and early developmental transitions to first-year fitness in a perennial tree species. This work demonstrates how ex situ collections can be used to identify climatically structured trait variation and guide conservation strategies aimed at maintaining adaptive potential under environmental change.

evolutionary biology↗

Variation in responses to temperature across admixed genotypes of Populus trichocarpa x P. balsamifera predict geographic shifts in regions where hybrids are favored

O_LIPlastic responses of plants to their environment vary as a result of genetic differentiation within and among species. To accurately predict rangewide responses to climate change, it is necessary to characterize genotype-specific reaction norms across the continuum of historic and future climate conditions comprising a species range. C_LIO_LIThe North American hybrid zone of Populus trichocarpa and P. balsamifera represents a natural system that has been shaped by climate, geography, and introgression. We leverage a dataset containing 45 clonal genotypes from this natural hybrid zone, planted across 17 replicated common garden experiments spanning a broad climatic range. Growth and mortality were measured over two years, enabling us to model reaction norms for each genotype across these tested environments. C_LIO_LISpecies ancestry and intraspecific genomic variation significantly influenced growth across environments, with genotypic variation in reaction norms reflecting a trade-off between cold tolerance and growth. Using modeled reaction norms for each genotype, we predicted that genotypes with more P. trichocarpa ancestry may gain an advantage under warmer climates. C_LIO_LISpatial shifts of the hybrid zone could facilitate the spread of beneficial alleles into novel climates. These results highlight that genotypic variation in responses to temperature will have landscape-level effects. C_LI

evolutionary biology↗

Synthetic auxotrophy reveals metabolic regulation of plasma cell generation, affinity maturation, and cytokine receptor signaling

The efficiencies with which activated B lymphocytes proliferate and develop into antibody (Ab)-secreting plasma cells are critical determinants of adaptive humoral immunity and sustain certain autoimmune diseases. Specific pathways in intermediary metabolism, or their substrate supply, influence lymphocyte differentiation and function. We now show that although stringent restriction of glutamine supply decreases proliferation and differentiation of B cells into plasma cells, glutaminolysis - a major means of metabolism of this amino acid - was only conditionally crucial in B cells and the Ab responses derived from them. Strikingly, Gls, the gene encoding the main glutaminase of lymphocytes, promoted anti-NP Ab responses at the primary and recall phases if either glucose uptake into B cells or pyruvate into their mitochondria was also impaired but otherwise was dispensable. This synthetic auxotrophy, i.e., conditional requirement of glutaminase for processes in addition to survival and proliferation, involved support to a progressive expansion of mitochondrial respiration followed by plasma cell differentiation. Surprisingly, impairment of glutaminase and the mitochondrial pyruvate channel decreased IL-21 stimulation of STAT3 phosphorylation as well as interferon stimulation of STAT1 activation. Together, our findings establish not only a powerful collaboration of metabolic pathways in programming increased respiration and the development of Ab-secreting cells, but also reveal modulation of cytokine receptor signaling by metabolism.

immunology↗

Genomics-driven monitoring of Fraxinus latifolia (Oregon Ash) for conservation and EAB-resistance breeding

Understanding the evolutionary processes underlying range-wide genomic variation is critical to designing effective conservation and restoration strategies. Evaluating the influence of connectivity, demographic change, and environmental adaptation for threatened species can be invaluable to proactive conservation of evolutionary potential. In this study, we assessed genomic variation across the range of Fraxinus latifolia, a foundational riparian tree native to western North America recently exposed to the invasive emerald ash borer (Agrilus planipennis; EAB). Over 1,000 individuals from 61 populations were sequenced using reduced representation (ddRAD-seq) across the species range. Strong population structure was evident along a latitudinal gradient, with population connectivity largely maintained along central valley river systems, and a center of diversity coinciding with major river systems central to the species range. Despite evidence of connectivity, estimates of nucleotide diversity and effective population size were low across all populations, suggesting the patchy distribution of F. latifolia populations may impact its long-term evolutionary potential. Range-wide estimates of genomic offset, which indicate genomic change required to adjust to future climate projections, were greatest in the eastern and lowest in the southern portions of the species range, suggesting the regional distribution of genomic variation may impact evolutionary potential longer-term. To preserve evolutionary capacity across populations needed for development of climate-resilient, EAB-resistant breeding programs, prioritizing conservation of range-wide genomic diversity will provide a foundation for species management long-term.

genomics↗

TRPV4 is expressed by enteric glia and muscularis macrophages of the colon but does not play a prominent role in colonic motility

BackgroundMechanosensation is an important trigger of physiological processes in the gastrointestinal tract. Aberrant responses to mechanical input are associated with digestive disorders, including visceral hypersensitivity. Transient Receptor Potential Vanilloid 4 (TRPV4) is a mechanosensory ion channel with proposed roles in visceral afferent signaling, intestinal inflammation, and gut motility. While TRPV4 is a potential therapeutic target for digestive disease, current mechanistic understanding of how TRPV4 may influence gut function is limited by inconsistent reports of TRPV4 expression and distribution. MethodsIn this study we profiled functional expression of TRPV4 using Ca2+ imaging of wholemount preparations of the mouse, monkey, and human intestine in combination with immunofluorescent labeling for established cellular markers. The involvement of TRPV4 in colonic motility was assessed in vitro using videomapping and contraction assays. ResultsThe TRPV4 agonist GSK1016790A evoked Ca2+ signaling in muscularis macrophages, enteric glia, and endothelial cells. TRPV4 specificity was confirmed using TRPV4 KO mouse tissue or antagonist pre-treatment. Calcium responses were not detected in other cell types required for neuromuscular signaling including enteric neurons, interstitial cells of Cajal, PDGFR+ cells, and intestinal smooth muscle. TRPV4 activation led to rapid Ca2+ responses by a subpopulation of glial cells, followed by sustained Ca2+ signaling throughout the enteric glial network. Propagation of these waves was suppressed by inhibition of gap junctions or Ca2+ release from intracellular stores. Coordinated glial signaling in response to GSK1016790A was also disrupted in acute TNBS colitis. The involvement of TRPV4 in the initiation and propagation of colonic motility patterns was examined in vitro. ConclusionsWe reveal a previously unappreciated role for TRPV4 in the initiation of distension-evoked colonic motility. These observations provide new insights into the functional role of TRPV4 activation in the gut, with important implications for how TRPV4 may influence critical processes including inflammatory signaling and motility. SummaryO_LITRPV4 is expressed by equivalent cell types in the rodent and primate (monkey and human) colon. This mechanosensitive ion channel has proposed roles in inflammation, visceral afferent signaling, and colonic motility. C_LIO_LINew analysis methods were developed to examine cellular communication in the enteric glial network. This approach revealed new insights into inflammation-associated changes in glial connectivity. C_LIO_LINew roles for TRPV4 in transduction of distension-evoked responses in the colon and colonic motility were identified. C_LI Key findingsWe have defined the cell types that functionally express TRPV4 in the gut wall. These include enteric glia, endothelia of blood and lymphatic vessels, mMac, and extrinsic afferent nerves. TRPV4- dependent Ca2+ signaling was not detected in enteric neurons, PDGFR cells, interstitial cells of Cajal and smooth muscle cells, which are important drivers of gut motility. These observations align with our experimental evidence for limited involvement of TRPV4 in neuromuscular transmission and propagating colonic motility. New and NoteworthyO_LINovel cellular sites of functional TRPV4 expression in the GI tract were identified and compared across multiple vertebrate species. New analytical approaches to characterize enteric glial communication in a spatiotemporal manner were developed. C_LIO_LIA supporting role for TRPV4 in the initiation of propagating colonic contractions in response to distension was demonstrated. Potential mechanisms that contribute to TRPV4-mediated effects on GI function were identified. C_LIO_LITRPV4-dependent activity in enteric glia is enhanced in inflammation, consistent with current evidence for inflammation-associated sensitization of TRPV4 on visceral afferents and a major role in mechanically evoked nociceptive signaling. C_LIO_LIPair correlation analysis was used to examine spatial connectivity of Ca2+ signaling, enabling demonstration of dysregulated glial communication in acute inflammation. C_LI

physiology↗

Climate and geography shape hybrid zone dynamics across space and time: insights from Populus trichocarpa x P. balsamifera

Population demographic changes, alongside landscape, geographic, and climate heterogeneity, can influence the timing, stability, and extent of introgression where species hybridize. Thus, quantifying interactions across diverged lineages, and the relative contributions of interspecific genetic exchange and selection to divergence at the genome-wide level is needed to better understand the drivers of hybrid zone formation and maintenance. We used seven latitudinally arrayed transects to quantify the contributions of climate, geography, and landscape features to broad patterns of genetic structure across the hybrid zone of Populus trichocarpa and P. balsamifera and evaluated the demographic context of hybridization over time. We found genetic structure differed among the seven transects. While ancestry was structured by climate, landscape features influenced gene flow dynamics. Demographic models indicated a secondary contact event may have influenced contemporary hybrid zone formation with the origin of a putative hybrid lineage that inhabits regions with higher aridity than either of the ancestral groups. Phylogenetic relationships based on chloroplast genomes support the origin of this hybrid lineage inferred from demographic models based on nuclear data. Our results point towards the importance of climate and landscape patterns in structuring the contact zones between P. trichocarpa and P. balsamifera and emphasize the value whole genome sequencing can have to advancing our understanding of how neutral processes influence divergence across space and time.

evolutionary biology↗

Chasing the fitness optimum: temporal variation in the genetic and environmental expression of life-history traits for a perennial plant

The ability of plants to track shifting fitness optima is crucial within the context of global change, where increasing environmental extremes may have dramatic consequences to life history, fitness, and ultimately species persistence. However, to track changing conditions relies upon the complex relationship between genetic and environmental variance, where selection may favor plasticity, the evolution of genetic differences, or both depending on the spatial and temporal scale of environmental heterogeneity. Over three years, we compared the genetic and environmental components of phenological and life-history variation in a common environment for the spring perennial Geum triflorum. Populations were sourced from alvar habitats that exhibit extreme, but predictable annual flood-desiccation cycles and prairie habitats that exhibit similar, but less predictable variation in water availability. Narrow-sense heritabilities were generally higher for early life history (emergence probability) relative to later life history traits (total seed mass), indicating that traits associated with establishment within an environment are under stronger genetic control relative to later life-history fitness expressions, where plasticity may play a larger role. This pattern was particularly notable in seeds sourced from environmentally extreme, but predictable alvar habitats relative to less predictable prairie seed sources. Fitness landscapes based on seed source origin, largely characterized by varying water availability and flower production, described selection as the degree of maladaptation to the prairie common garden environment relative to seed source environment. Plants from alvar populations were consistently closer to the fitness optimum across all years. Annually, the breadth of the fitness optimum expanded primarily along a moisture gradient, with inclusion of more populations onto the expanding optimum. These results highlight the importance of temporally and spatially varying selection for the evolution of life history, indicating plasticity within perennial systems may over time become the primary mechanism to track fitness for later life history events.

evolutionary biology↗

Reduced representation sequencing to understand the evolutionary history of Torrey pine (Pinus torreyana Parry) with implications for rare species conservation

Understanding the contribution of neutral and adaptive evolutionary processes to population differences is often necessary for better informed management and conservation of rare species. In this study, we focused on Pinus torreyana Parry (Torrey pine), one of the worlds rarest pines, endemic to one island and one mainland population in California. Small population size, low genetic diversity, and susceptibility to abiotic and biotic stresses suggest Torrey pine may benefit from inter-population genetic rescue to preserve the species evolutionary potential. We leveraged reduced representation sequencing to tease apart the respective contributions of stochastic and deterministic evolutionary processes to population differentiation. We applied these data to model spatial and temporal demographic changes in effective population sizes and genetic connectivity, to assess loci possibly under selection, and evaluate genetic rescue as a potential conservation strategy. Overall, we observed exceedingly low standing variation reflecting consistently low effective population sizes across time and limited genetic differentiation suggesting maintenance of gene flow following divergence. However, genome scans identified more than 2000 SNPs candidates for divergent selection. Combined with previous observations indicating population phenotypic differentiation, this indicates that natural selection has likely contributed to population genetic differences. Thus, while reduced genetic diversity, small effective population size, and genetic connectivity between populations suggest genetic rescue could mitigate the adverse effect of rarity, divergent selection between populations indicates that genetic mixing could disrupt adaptation. Further work evaluating the fitness consequences of inter-population admixture is necessary to empirically evaluate the trade-offs associated with genetic rescue in Torrey pine.

genomics↗

Seed morphology and emergence variability in a conservation collection of Pinus torreyana

BackgroundUnderstanding the within- and among-population distribution of trait variation within seed collections may provide a means to approximate standing genetic variation and inform plant conservation. AimsThis study aimed to estimate population- and family-level seed trait variability for existing seed collections of Torrey pine (Pinus torreyana), and to use these data to guide sampling of future collections. MethodsWe quantified variation in 14 seed morphological traits and seedling emergence within and among Torrey pine populations. Using a simulation-based approach, we used estimates of within-population variance to assess the number of maternal families required to capture 95% of trait variation within each existing seed collection. ResultsSubstantial structure was observed both within and among Torrey pine populations, with island and mainland seeds varying in seed size and seed coat thickness. Despite morphological differences, seedling emergence was similar across populations. Simulations revealed that 83% and 71% of all maternal families within island and mainland seed collections respectively needed to be resampled to capture 95% of seed trait variation within existing collections. ConclusionsFrom a conservation perspective, our results indicate that to optimize genetic diversity captured in Torrey pine seed collections, maximizing the number of maternal families sampled within each population will be necessary.

plant biology↗

Local climate and habitat continuity interact to alter contemporary dispersal potential

Understanding the evolution of dispersal under changing global environments is essential to predicting a species ability to track shifting ecological niches. Two important, but anthropogenically altered, sources of selection on dispersal are climate and habitat continuity. Despite the likelihood these global drivers of selection act simultaneously on plant populations, their combined effects on dispersal are rarely examined. To understand the interactive effect of climate and habitat continuity on dispersal potential, we study Geum triflorum - a perennial grassland species that spans a wide range of environments, including both continuous prairie and isolated alvar habitats. We explore how the local climate of the growing season and habitat continuity (continuous vs isolated) interact to alter dispersal potential. We find a consistent interactive effect of local climate and habitat continuity on dispersal potential. Across continuous prairie populations, an increased number of growing degree days favors traits that increase dispersal potential. However, for isolated alvar populations, dispersal potential tends to decrease as the number of growing degree days increase. Our findings suggest that under continued warming, populations in continuous habitats will benefit from increased gene flow, while isolated populations will become increasingly segregated, with reduced potential to track shifting fitness optima.

evolutionary biology↗

Environmental and geographic data optimize ex situ collections and the preservation of adaptive evolutionary potential

Maintenance of biodiversity, through seed banks and botanical gardens where the wealth of species genetic variation may be preserved ex situ, is a major goal of conservation. However, challenges can persist in optimizing ex situ collections where trade-offs exist between expense, effort, and conserving species evolutionary potential, particularly when genetic data is not available. Within this context, we evaluate the genetic consequences of guiding population preservation using geographic (isolation-by-distance, IBD) and environmental (isolation-by-environment, IBE) data for ex situ collections where provenance data is available. We use 19 genetic and genomic datasets from 15 plant species to (i) assess the proportion of population genetic differentiation explained by geographic and environmental factors, and (ii) simulate ex situ collections prioritizing source populations based on pairwise geographic or environmental distances. Specifically, we test the impact prioritizing sampling based on environmental and geographic distances may have on capturing neutral, functional or putatively adaptive genetic diversity and differentiation. We find that collectively IBD and IBE explain a substantial proportion of genetic differences among functional (median 45%) and adaptive (median 71%) loci, but not for neutral loci (median 21.5%). Simulated ex situ collections reveal that inclusion of IBD and IBE increases both allelic diversity and genetic differentiation captured among populations, particularly for loci that may be important for adaptation. Thus, prioritizing population collections using environmental and geographic distance data can impact genetic variation captured ex situ. This provides value for the vast majority of plant species for which we have no genetic data, informing conservation of genetic variation needed to maintain evolutionary potential within collections.

genomics↗